Thrombospondin-4, tumour necrosis factor-like weak inducer of apoptosis (TWEAK) and its receptor Fn14: Novel extracellular matrix modulating factors in cardiac remodelling

Annals of Medicine

Volumn 44, Issue 8, 2012, Pages 793-804

  Mustonen, Erja ^a   Ruskoaho, Heikki ^a   Rysä, Jaana ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

Cardiac remodelling; Extracellular matrix protein; Fn14; Left ventricular hypertrophy; Myocardial infarction; Thrombospondin; TWEAK

Indexed keywords

COLLAGEN; CYTOKINE; FN14; THROMBOSPONDIN; THROMBOSPONDIN 4; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

CARDIAC REMODELLING; EXTRACELLULAR MATRIX; FIBROBLAST; HEART DISEASE; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE OVERLOAD; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; EXTRACELLULAR MATRIX; FIBROSIS; HUMANS; MYOCARDIUM; RECEPTORS, TUMOR NECROSIS FACTOR; THROMBOSPONDINS; TUMOR NECROSIS FACTORS; VENTRICULAR REMODELING;

EID: 84870781105     PISSN: 07853890     EISSN: 13652060     Source Type: Journal    
DOI: 10.3109/07853890.2011.614635     Document Type: Review

References (94)

1. Cohn JN, Ferrari R, Sharpe N. Cardiac remodeling-concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling. J Am Coll Cardiol. 2000;35:569-82.
2. Hill JA, Olson EN. Cardiac plasticity. N Engl J Med. 2008; 358:1370-80.
3. Brown RD, Ambler SK, Mitchell MD, Long CS. The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Annu Rev Pharmacol Toxicol. 2005;45: 657-87.
4. Porter KE, Turner NA. Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther. 2009;123: 255-78.
5. Eyden B. The myofibroblast: phenotypic characterization as a prerequisite to understanding its functions in translational medicine. J Cell Mol Med. 2008;12:22-37.
6. Baudino TA, Carver W, Giles W, Borg TK. Cardiac fibroblasts: friend or foe? Am J Physiol Heart Circ Physiol. 2006; 291:H1015-26.
7. Berk BC, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Invest. 2007;117:568-75.
8. Fedak PW, Verma S, Weisel RD, Li RK. Cardiac remodeling and failure: from molecules to man (Part II). Cardiovasc Pathol. 2005;14:49-60.
9. Graham HK, Horn M, Trafford AW. Extracellular matrix profiles in the progression to heart failure. European Young Physiologists Symposium Keynote Lecture-Bratislava 2007. Acta Physiol (Oxf). 2008;194:3-21.
10. Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol. 2002; 14:608-16.
11. Fedak PW, Verma S, Weisel RD, Li RK. Cardiac remodeling and failure: from molecules to man (Part I). Cardiovasc Pathol. 2005;14:1-11.
12. Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol. 2010;48:504-11.
13. Jugdutt BI. Remodeling of the myocardium and potential targets in the collagen degradation and synthesis pathways. Curr Drug Targets Cardiovasc Haematol Disord. 2003;3: 1-30.
14. Jane-Lise S, Corda S, Chassagne C, Rappaport L. The extracellular matrix and the cytoskeleton in heart hypertrophy and failure. Heart Fail Rev. 2000;5:239-50.
15. Manabe I, Shindo T, Nagai R. Gene expression in fibroblasts and fibrosis: involvement in cardiac hypertrophy. Circ Res. 2002;91:1103-13.
16. Corda S, Samuel JL, Rappaport L. Extracellular matrix and growth factors during heart growth. Heart Fail Rev. 2000; 5:119-30.
17. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007;87:1285-342.
18. Li YY, McTiernan CF, Feldman AM. Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiac matrix remodeling. Cardiovasc Res. 2000;46:214-24.
19. Bernardo BC, Weeks KL, Pretorius L, McMullen JR. Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol Ther. 2010;128:191-227.
20. Brower GL, Gardner JD, Forman MF, Murray DB, Voloshenyuk T, Levick SP, et al. The relationship between myocardial extracellular matrix remodeling and ventricular function. Eur J Cardiothorac Surg. 2006;30:604-10.
21. Jugdutt BI. Ventricular remodeling after infarction and the extracellular collagen matrix: when is enough enough? Circulation. 2003;108:1395-403.
22. Janicki JS, Brower GL. The role of myocardial fibrillar collagen in ventricular remodeling and function. J Card Fail. 2002;8:S319-25.
23. Lopez B, Gonzalez A, Hermida N, Valencia F, de Teresa E, Diez J. Role of lysyl oxidase in myocardial fibrosis: from basic science to clinical aspects. Am J Physiol Heart Circ Physiol. 2010;299:H1-9.
24. Zieman S, Kass D. Advanced glycation end product crosslinking: pathophysiologic role and therapeutic target in cardiovascular disease. Congest Heart Fail. 2004;10:144-9; quiz 150-1.
25. Gunja-Smith Z, Morales AR, Romanelli R, Woessner JF Jr. Remodeling of human myocardial collagen in idiopathic dilated cardiomyopathy. Role of metalloproteinases and pyridinoline cross-links. Am J Pathol. 1996;148:1639-48.
26. W oodiwiss AJ, Tsotetsi OJ, Sprott S, Lancaster EJ, Mela T, Chung ES, et al. Reduction in myocardial collagen crosslinking parallels left ventricular dilatation in rat models of systolic chamber dysfunction. Circulation. 2001;103: 155-60.
27. Frangogiannis NG. Targeting the inflammatory response in healing myocardial infarcts. Curr Med Chem. 2006;13: 1877-93.
28. Baumgarten G, Knuefermann P, Kalra D, Gao F, Taffet GE, Michael L, et al. Load-dependent and-independent regulation of proinflammatory cytokine and cytokine receptor gene expression in the adult mammalian heart. Circulation. 2002;105:2192-97.
29. Xia Y, Lee K, Li N, Corbett D, Mendoza L, Frangogiannis NG. Characterization of the inflammatory and fibrotic response in a mouse model of cardiac pressure overload. Histochem Cell Biol. 2009;131:471-81.
30. Celis R, Torre-Martinez G, Torre-Amione G. Evidence for activation of immune system in heart failure: is there a role for anti-inflammatory therapy? Curr Opin Cardiol. 2008;23: 254-60.
31. Levine B, Kalman J, Mayer L, Fillit HM, Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N Engl J Med. 1990;323:236-41.
32. Seta Y, Shan K, Bozkurt B, Oral H, Mann DL. Basic mechanisms in heart failure: the cytokine hypothesis. J Card Fail. 1996;2:243-49.
33. Mann DL. Stress-activated cytokines and the heart: from adaptation to maladaptation. Annu Rev Physiol. 2003;65: 81-101.
34. Frangogiannis NG. The immune system and cardiac repair. Pharmacol Res. 2008;58:88-111.
35. Dreyer WJ, Michael LH, Nguyen T, Smith CW, Anderson DC, Entman ML, et al. Kinetics of C5a release in cardiac lymph of dogs experiencing coronary artery ischemiareperfusion injury. Circ Res. 1992;71:1518-24.
36. Schellings MW, Pinto YM, Heymans S. Matricellular proteins in the heart: possible role during stress and remodeling. Cardiovasc Res. 2004;64:24-31.
37. Schellings MW, van Almen GC, Sage EH, Heymans S. Thrombospondins in the heart: potential functions in cardiac remodeling. J Cell Commun Signal. 2009;3:201-13.
38. Adams JC. Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol. 2001;17:25-51.
39. Adams JC, Lawler J. The thrombospondins. Int J Biochem Cell Biol. 2004;36:961-8.
40. Frangogiannis NG, Ren G, Dewald O, Zymek P, Haudek S, Koerting A, et al. Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts. Circulation. 2005;111:2935-42.
41. Swinnen M, Vanhoutte D, Van Almen GC, Hamdani N, Schellings MW, D' hooge J, et al. Absence of thrombospondin-2 causes age-related dilated cardiomyopathy. Circulation. 2009;120:1585-97.
42. Blankesteijn WM, Creemers E, Lutgens E, Cleutjens JP, Daemen MJ, Smits JF. Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice. Acta Physiol Scand. 2001;1731:75-82.
43. Schroen B, Heymans S, Sharma U, Blankesteijn WM, Pokharel S, Cleutjens JP, et al. Thrombospondin-2 is essential for myocardial matrix integrity: increased expression identifies failure-prone cardiac hypertrophy. Circ Res. 2004;95: 515-22.
44. Adolph KW. Relative abundance of thrombospondin 2 and thrombospondin 3 mRNAs in human tissues. Biochem Biophys Res Commun. 1999;258:792-6.
45. Tan FL, Moravec CS, Li J, Apperson-Hansen C, McCarthy PM, Young JB, et al. The gene expression fingerprint of human heart failure. Proc Natl Acad Sci USA. 2002;99: 11387-92.
46. Gabrielsen A, Lawler PR, Yongzhong W, Steinbruchel D, Blagoja D, Paulsson-Berne G, et al. Gene expression signals involved in ischemic injury, extracellular matrix composition and fibrosis defined by global mRNA profiling of the human left ventricular myocardium. J Mol Cell Cardiol. 2007;42: 870-83.
47. Rys ä J, Leskinen H, Ilves M, Ruskoaho H. Distinct upregulation of extracellular matrix genes in transition from hypertrophy to hypertensive heart failure. Hypertension. 2005;45: 927-33.
48. Moens AL, Cingolani O, Spinale FS, Kass DA. Exacerbated cardiac remodeling to pressure-overload in mice lacking thrombospondin-4. Hypertension. 2008;52:747-75.
49. Frolova E, Sopko N, Penn M, Stenina O, Plow E. Heart hypertrophy in response to pressure overload in TSP4 knockout mice. FASEB J. 2009;23(Meeting Abstracts):642. 5-642.5.
50. Narouz-Ott L, Maurer P, Nitsche DP, Smyth N, Paulsson M. Thrombospondin-4 binds specifically to both collagenous and non-collagenous extracellular matrix proteins via its C-terminal domains. J Biol Chem. 2000;275:37110-7.
51. Sodersten F, Ekman S, Niehoff A, Zaucke F, Heinegard D, Hultenby K. Ultrastructural immunolocalization of cartilage oligomeric matrix protein, thrombospondin-4, and collagen fibril size in rodent achilles tendon in relation to exercise. Connect Tissue Res. 2007;48:254-62.
52. Halasz K, Kassner A, Morgelin M, Heinegard D. COMP acts as a catalyst in collagen fibrillogenesis. J Biol Chem. 2007;282:31166-73.
53. Mustonen E, Aro J, Puhakka J, Ilves M, Soini Y, Leskinen H, et al. Thrombospondin-4 expression is rapidly upregulated by cardiac overload. Biochem Biophys Res Commun. 2008;373:186-91.
54. Stenina OI, Desai SY, Krukovets I, Kight K, Janigro D, Topol EJ, et al. Thrombospondin-4 and its variants: expression and differential effects on endothelial cells. Circulation. 2003;108:1514-9.
55. Zhao XM, Hu Y, Miller GG, Mitchell RN, Libby P. Association of thrombospondin-1 and cardiac allograft vasculopathy in human cardiac allografts. Circulation. 2001;103: 525-31.
56. Sezaki S, Hirohata S, Iwabu A, Nakamura K, Toeda K, Miyoshi T, et al. Thrombospondin-1 is induced in rat myocardial infarction and its induction is accelerated by ischemia/reperfusion. Exp Biol Med (Maywood). 2005;230:621-30.
57. Mustonen E, Leskinen H, Aro J, Luodonp ä ä M, Vuolteenaho O, Ruskoaho H, et al. Metoprolol treatment lowers thrombospondin-4 expression in rats with myocardial infarction and left ventricular hypertrophy. Basic Clin Pharmacol Toxicol. 2010;107:709-17.
58. Fang C, Carlson CS, Leslie MP, Tulli H, Stolerman E, Perris R, et al. Molecular cloning, sequencing, and tissue and developmental expression of mouse cartilage oligomeric matrix protein (COMP). J Orthop Res. 2000;18:593-603.
59. Kipnes JR, Xu L, Han F, Rallapalli R, Jimenez S, Hall DJ, et al. Molecular cloning and expression patterns of mouse cartilage oligomeric matrix protein gene. Osteoarthritis Cartilage. 2000;8:236-9.
60. Svensson L, Aszó d i A, Heinegå r d D, Hunziker EB, Reinholt FB, F ä ssler R, et al. Cartilage oligomeric matrix protein-deficient mice have normal skeletal development. Mol Cell Biol. 2002;22:4366-71.
61. Bornstein P, Agah A, Kyriakides TR. The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int J Biochem Cell Biol. 2004;36:1115-25.
62. Frolova E, Pluskota E, Krukovets I, Burke T, Drumm C, Smith JD, et al. Thrombospondin-4 regulates vascular inflammation and atherogenesis. Circ Res. 2010;107: 1313-25.
63. Chicheportiche Y, Bourdon PR, Xu H, Hsu YM, Scott H, Hession C, et al. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem. 1997;272;51:32401-10.
64. Brown SA, Ghosh A, Winkles JA. Full-length, membraneanchored TWEAK can function as a juxtacrine signaling molecule and activate the NF-kappaB pathway. J Biol Chem. 2010;285:17432-41.
65. Meighan-Mantha RL, Hsu DK, Guo Y, Brown SA, Feng SL, Peifley KA, et al. The mitogen-inducible Fn14 gene encodes a type I transmembrane protein that modulates fibroblast adhesion and migration. J Biol Chem. 1999;274: 33166-76.
66. Wiley SR, Cassiano L, Lofton T, Davis-Smith T, Winkles JA, Lindner V, et al. A novel TNF receptor family member binds TWEAK and is implicated in angiogenesis. Immunity. 2001;155:837-46.
67. Chorianopoulos E, Heger T, Lutz M, Frank D, Bea F, Katus HA, et al. FGF-inducible 14-kDa protein (Fn14) is regulated via the RhoA/ROCK kinase pathway in cardiomyocytes and mediates nuclear factor-kappaB activation by TWEAK. Basic Res Cardiol. 2010;105:301-13.
68. Jain M, Jakubowski A, Cui L, Shi J, Su L, Bauer M, et al. A novel role for tumor necrosis factor-like weak inducer of apoptosis (TWEAK) in the development of cardiac dysfunction and failure. Circulation. 2009;119:2058-68.
69. Feng SL, Guo Y, Factor VM, Thorgeirsson SS, Bell DW, Testa JR, et al. The Fn14 immediate-early response gene is induced during liver regeneration and highly expressed in both human and murine hepatocellular carcinomas. Am J Pathol. 2000;156:1253-61.
70. Winkles JA. The TWEAK-Fn14 cytokine-receptor axis: discovery, biology and therapeutic targeting. Nat Rev Drug Discov. 2008;75:411-25.
71. Burkly LC, Michaelson JS, Hahm K, Jakubowski A, Zheng TS. TWEAKing tissue remodeling by a multifunctional cytokine: role of TWEAK/Fn14 pathway in health and disease. Cytokine. 2007;40:1-16.
72. Mustonen E, S äk kinen H, Tokola H, Isopoussu E, Aro J, Leskinen H, et al. Tumour necrosis factor-like weak inducer of apoptosis (TWEAK) and its receptor Fn14 during cardiac remodelling in rats. Acta Physiol (Oxf). 2010;199: 11-22.
73. Chorianopoulos E, Rosenberg M, Zugck C, Wolf J, Katus HA, Frey N. Decreased soluble TWEAK levels predict an adverse prognosis in patients with chronic stable heart failure. Eur J Heart Fail. 2009;11:1050-6.
74. Richter B, Rychli K, Hohensinner PJ, Berger R, Mortl D, Neuhold S, et al. Differences in the predictive value of tumor necrosis factor-like weak inducer of apoptosis (TWEAK) in advanced ischemic and non-ischemic heart failure. Atherosclerosis. 2010;213:545-8.
75. Chorianopoulos E, Jarr K, Steen H, Giannitsis E, Frey N, Katus HA. Soluble TWEAK is markedly upregulated in patients with ST-elevation myocardial infarction and related to an adverse short-term outcome. Atherosclerosis. 2010;211: 322-26.
76. Meyer T, Amaya M, Desai H, Robles-Carrillo L, Hatfield M, Francis JL, et al. Human platelets contain and release TWEAK. Platelets. 2010;21:571-4.
77. Maecker H, Varfolomeev E, Kischkel F, Lawrence D, LeBlanc H, Lee W, et al. TWEAK attenuates the transition from innate to adaptive immunity. Cell. 2005;123:931-44.
78. Jakubowski A, Ambrose C, Parr M, Lincecum JM, Wang MZ, Zheng TS, et al. TWEAK induces liver progenitor cell proliferation. J Clin Invest. 2005;115:2330-40.
79. Mittal A, Bhatnagar S, Kumar A, Lach-Trifilieff E, Wauters S, Li H, et al. The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice. J Cell Biol. 2010;188:833-49.
80. Ortiz A, Sanz AB, Munoz Garcia B, Moreno JA, Sanchez Nino MD, Martin-Ventura JL, et al. Considering TWEAK as a target for therapy in renal and vascular injury. Cytokine Growth Factor Rev. 2009;20:251-8.
81. Hotta K, Sho M, Yamato I, Shimada K, Harada H, Akahori T, et al. Direct targeting of fibroblast growth factor-inducible 14 protein protects against renal ischemia reperfusion injury. Kidney Int. 2011;79:179-88.
82. Li H, Mittal A, Paul PK, Kumar M, Srivastava DS, Tyagi SC, et al. Tumor necrosis factor-related weak inducer of apoptosis augments matrix metalloproteinase 9 (MMP-9) production in skeletal muscle through the activation of nuclear factor-B-inducing kinase and p38 mitogenactivated protein kinase: a potential role of MMP-9 in myopathy. J Biol Chem. 2009;284:4439-50.
83. D ogra C, Hall SL, Wedhas N, Linkhart TA, Kumar A. Fibroblast growth factor inducible 14 (Fn14) is required for the expression of myogenic regulatory factors and differentiation of myoblasts into myotubes. Evidence for TWEAKindependent functions of Fn14 during myogenesis. J Biol Chem. 2007;282:15000-10.
84. Bover LC, Cardo-Vila M, Kuniyasu A, Sun J, Rangel R, Takeya M, et al. A previously unrecognized protein-protein interaction between TWEAK and CD163: potential biological implications. J Immunol. 2007;178:8183-94.
85. Polek TC, Talpaz M, Darnay BG, Spivak-Kroizman T. TWEAK mediates signal transduction and differentiation of RAW264.7 cells in the absence of Fn14/TweakR. Evidence for a second TWEAK receptor. J Biol Chem. 2003;278:32317-23.
86. De Ketelaere A, Vermeulen L, Vialard J, Van De Weyer I, Van Wauwe J, Haegeman G, et al. Involvement of GSK-3-beta in TWEAK-mediated NF-kappaB activation. FEBS Lett. 2004;566:60-4.
87. Heymans S, Hirsch E, Anker SD, Aukrust P, Balligand JL, Cohen-Tervaert JW, et al. Inflammation as a therapeutic target in heart failure? A scientific statement from the Translational Research Committee of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail. 2009;112:119-29.
88. Bornstein P. Thrombospondins function as regulators of angiogenesis. J Cell Commun Signal. 2009;3:189-200.
89. Carlson CB, Lawler J, Mosher DF. Structures of thrombospondins. Cell Mol Life Sci. 2008;65:672-86.
90. Wiley SR, Winkles JA. TWEAK, a member of the TNF superfamily, is a multifunctional cytokine that binds the TweakR/Fn14 receptor. Cytokine Growth Factor Rev. 2003; 14:241-9.
91. Lawler J, Duquette M, Whittaker CA, Adams JC, McHenry K, DeSimone DW. Identification and characterization of thrombospondin-4, a new member of the thrombospondin gene family. J Cell Biol. 1993:120;1059-67.
92. Wang D, Oparil S, Feng JA, Li P, Perry G, Chen LB, et al. Effects of pressure overload on extracellular matrix expression in the heart of the atrial natriuretic peptide-null mouse. Hypertension. 2003;42:88-95.
93. Zhang XM, Shen F, Xv ZY, Yan ZY, Han S. Expression changes of thrombospondin-1 and neuropeptide Y in myocardium of STZ-induced rats. Int J Cardiol. 2005;105: 192-7.
94. van Almen GC, Swinnen M, Carai P, Verhesen W, Cleutjens JP, D' hooge J, et al. Absence of thrombospondin-2 increases cardiomyocyte damage and matrix disruption in doxorubicin-induced cardiomyopathy. J Mol Cell Cardiol. 2011;51:318-28.